Symbiosis, 30 (2001) 83-96Balaban, Philadelphia/Rehovot

83

Review articleSymbiosis and Competition: Complex InteractionsAmong Beetles, Fungi and Mites

K.D. KLEPZIGl*, J.C. MOSERl, F.J. LOMBARDER02, R.W. HOFSTETTERgand M.P. AYRES31USDA Forest Service, 2500 Shreveport Hwy., Pineville, LA 71360, USATel. +I-318-473-7238, Fax. +I-318-473-7222, E-mail. kklepzig@fsfed.us;2Departamen to de Produccion Vegetal, Universidad de Santiago, EscuelaPolitecnica Superior, Campus de Lugo, 27002 Spain, Tel. +34-982-252231,Fax. +34-982-241835, E-mail. flombard@lugo.usc.es;3Department of Biological Sciences, Dartmouth College, Hanover, NH 03755,USA, Tel. +I-603-646-2788, Fax. +l-603-646-1347,E-mail. Matthew.P.Ayres@Dartmouth.EDU

Received August 14,200O; Accepted November 4,200O

AbstractSymbioses among bark beetles and their fungal and mite associates involve

complex, multi-level interactions. Dendroctonus frontalis attacks and kills southernpines , introducing fungi into the tree . Ophiostoma minus , may in i t ia l ly a id beet les inki l l ing trees , but later this “bluestain” fungus becomes an antagonist , competing withlarvae for host phloem. Two additional fungi, Entomocorticium sp. A andCeratocystiopsis ranaculosus are carried within a specialized mycangium andinoculated into phloem where they are fed upon by beetle larvae. The beetle alsovectors several species of phoretic mites which transport spores of 0 . minus and C.ranaculosus and can complete their life cycle upon these two fungi. A similarinteraction occurs between Ips avuZsus and its fungal (Entomocorticium spp.) andmite (Eluttoma bennetti) symbionts. Larval beetles feed on fungus as do the mites.

Presented at the 3rd lntemational Congress on Symbios is , Aug. 13-19, 2000, Marburg, Germany

*The author to whom correspondence should be sent.

0334-5114/2001/$05.50 02001 Balaban

84 K.D. KLEPZIG ET AL.

Female mites feed on fungus growing within beet le gal ler ies , swel l ing to many t imestheir normal s ize. Larval mites develop and mate within the females who burst open,giving birth to reproductively mature females. These relationships may be bestunderstood by considering the manner in which symbioses vary with time andresources, and the degree to which other species may affect interactions amongsymbionts .

Keywords: Insect , fungus, mite , competi t ion, bark beet le , Ophiostoma, s y m b i o s i s

1. Introduction

Symbiosis may be defined as the “Acquisition and maintenance of one or moreorganisms by another that results in novel structures and (or) metabolism”(Zook, 1998) (”or” added by authors). We consider herein two complexillustrations of symbiosis between tree killing bark beetles and the fungi andmites they carry.

While others have reviewed the biology and ecology of bark beetle-fungalinteractions (Malloch and Blackwell, 1993; Paine et al., 1997), gaps stillremain in our knowledge of the relative benefits accrued by the participants inthese symbiotic interactions, and key biological details remain unrevealed.We have focused on interactions between a tree killing bark beetle(Dendroctonus frontalis) the fungi it vectors, and the phoretic mites it carries.We will briefly consider the interactions in this system (those seeking a morethorough consideration of the topic are directed to Klepzig and Wilkens, 1997;Lombardero et al., 2000; and Klepzig et al., 2000), and then reveal newinformation pertaining to another symbiotic interaction, that between a lessaggressive*bark beetle (Ips avulsus), the fungus it vectors and one of the mites itcarries.

2. The Southern Pine Beetle

Dendroctonus frontalis Zimmermann (Coleoptera:Scolytidae) (Fig. la) is themost damaging forest insect in the southern United States (Thatcher et al.,1980; Drooz, 1985; Price et al., 1992). This beetle mounts mass attacks (initiatedby females with the use of aggregation pheromones) and kills healthy trees(Paine et al., 1997). Mated female beetles chew egg galleries within the innerbark and phloem (Thatcher, 1960; Payne, 1983), inoculating several fungi in theprocess (Bramble and Holst, 1940) including Ophiostoma minus (Hedge.) H. andI’. Sydow, Entomocorticium sp. A (an undescribed basidiomycete, formerlyreferred to in the literature as isolate SJB122), and Ceratocysfiopsis

BEETLES, FUNGI, AND MITES 85

~unaculosus Perry and Bridges. 0. minus is an ascomycetous fungus which causes“bluestain” within infected wood and is carried phoretically on the D.frontalis exoskeleton (Rumbold, 1931; Bridges and Moser, 1983) and by phoreticmites (Bridges and Moser, 1983; discussed in detail below). While this fungusmay aid D. frontalis in killing trees (Nelson, 1934; Caird, 1935; Bramble andHolst, 1940; Mathre, 1964; Basham, 1970), it is not required for tree death tooccur (Hetrick, 1949; Bridges, 1985; Bridges et al., 1985). Colonization by 0.minus may, however, cause tree death to occur more quickly or at leastdifferently than it would in the absence of the fungus (Paine et al., 1997).Because of this, and because the fungus benefits by receiving transport to newhost tissue (Dowding, 1969), the D. frontalis -0. minus relationship - at theearly stages of attack - may be defined as a mutualistic symbiosis. However, asbeetle eggs hatch, the introduced fungi grow and colonize the phloem. Whencolonization by 0. minus overlaps areas of larval feeding, reduceddevelopmental success - inhibited egg production, slower larval growth anddevelopment, and increased mortality - may occur (Barras, 1970; Franklin,1970), and higher levels of 0. minus thus correlate with lowered D. frontalisreproductive success (Lombardero et al., 2000). This antagonism between 0.minus and D. frontalis larvae is due to interference by the fungus withinteractions between the beetle and its two mutualistic fungi (Klepzig et al.,2000).

Each female D. frontalis possesses a prothoracic mycangium consisting ofpaired invaginations of the exoskeleton each of which has one pore-likeventral opening and contains two types of secretory cells (Barras and Perry,1972; Happ et al., 1971). Within each side of the mycangium, the femalemaintains a pure culture of either C. runuculosus (Barras and Taylor, 1973) orEntomocorticium sp. A (Barras and Perry, 1972; Happ et al., 1976; Hsiau, 1996).Each female may carry either one (rarely both) of the two fungi, or no fungi, ineither of the two mycangial pouches (Bridges, 1985). As the female ovipositswithin the tree, she may inoculate the area immediately surrounding the eggswith the contents of her mycangium. Early instar larvae feed within shortgalleries which quickly enlarge into obovate feeding chambers (Fig. lb)(Payne, 1983) within which can be found abundant growth and sporulation ofeither of the two mycangial fungi. The larvae likely then feed on fungalhyphae and spores, receiving the majority of their nutrition (especially N)from the fungi and substantially benefit from the presence of these fungi(Bridges, 1985; Goldhammer et al., 1990; Coppedge et al., 1995; Ayres et al.,2000). The mycangial fungi receive protected, selective transport to the nextavailable resource (Happ et al., 1971). The symbiosis between these organismsis clearly mutualistic (Klepzig et al., 2000).

In addition, over 96 species of mites are associated with D. frontalis (Moserand Roton, 1971). Among these associates are parasites, predators, fungivores

K.D. KLEPZIC ; ET AL.

.

Figure 1. Southern pine beetle, Dendroctonusfrontalis. A) Flying adult beetles, B)galleries of larvae.

and omnivores (Moser and Roton, 1971; Moser et al., 1971, 1974). Of tl lese, atleast 14 species may be phoretic (Moser and Roton, 1971) in which the mite istransported on the external surface of the beetle and does not undergo fee ding orontogenesis during this period of transport (Lindquist, 1969; Smiley and Moser,

feeding

BEETLES, FUNGI, AND MITES

Figure 2. Tarsonemus sp. mite with flap like sporothecae (located on both sides of mcontaining ascospores of Ceratocyst iopsis ranaculosus.

ki te )

Figure 3. Primary resource capture competit ive interactions between A) Ophiostoma minusand Ceratocyst iopsis ranaculosus, B) Ophiostoma minus and Entomocort ic ium sp.A., and, C) Ceratocyst iopsis ranaculosus and Entomocort ic ium sp. A.

88 K.D. KLEPZIG ET AL.

1974). In particular, three Tursonemus spp. - 7’. ips Lindquist, T. krurzfzii Smileyand Moser, and T. fisarii Cooreman (Moser and Roton, 1971; Smiley and Moser,1974; Moser, 1976; Bridges and Moser, 1983; Moser and Bridges, 1986) arephoretic on D. frontalis, obtaining transport to host material with no directlydeleterious effects on the beetle. However, the mites do appear to indirectlyimpact the D. frontalis-fungus-tree interaction (Lombardero et al., 2000;Klepzig et al., 2000). All three mites possess specialized, flap-like structuresof the integument (Fig. 2). In T. ips and T. kranfzii, these sporothecaefrequently contain 0. minus and C. runuculosus ascospores (Bridges and Moser,1983; Moser, 1985; Moser et al., 1995). Contributing to the complexity of thisinteraction, are the differential competitive capabilities of the D. frontalisassociated fungi within host tree tissue.

0. minus, Enfomocorficium sp. A, and C. ranaculosus, compete for uncolonizedpine phloem. In competition experiments on uncolonized natural and artificialsubstrates the superior competitor is always 0. minus, whose rapid growth rateand aggressive resource capture tactics overwhelm the mycangial fungi inprimary resource capture (Klepzig and Wilkens, 1997). Enfomocorficium sp. A.and C. runuculosus are similar in their relative competitive abilities,suggesting a lack of differential competition. When direct confrontations occurbetween the fungi, the two mycangial fungi noticeably differ in theircompetitive abilities. 0. minus quickly grows over C. ranaculosus colonies andcaptures the resource already held by this fungus. In contrast, direct interactionwith Enfomocorficium sp. A slows 0. minus drastically. If 0. minus grows aftercoming into contact with this fungus, it grows around the colony, never growingover the basidiomycete and never capturing the resource it holds (Fig. 3). Thislimitation on the growth and further spread of 0. minus suggests either closerange antibiotic production or localized nutrient depletion by En fomocorficiumsp. A. It is important to consider, though, that these interactions are likely notstatic and that they may change in trees as environmental (abiotic) factorschange (Callaway and Walker, 1997).

0. minus is clearly best able to colonize the phloem available in the earlystages of D. frontalis attack, due especially to its rapid growth and relativelyhigh tolerance of pine allelochemicals (Bridges, 1987). If 0. minus does assistin killing trees, this is advantageous to the beetle and disadvantageous to thetree. As female beetles begin inoculating the mycangial fungi into the phloemof the attacked tree, the aggressively saprophytic characteristics of 0. minusmay become a disadvantage for D. frontalis. At this point, the female needs toestablish colonies of the mycangial fungi to serve as a larval food source. C.ranaculosus, grows faster than Enfomocorficium sp. A. but is not capable ofexcluding growth of 0. minus enough to allow larval development (Klepzig andWilkens, 1997). Given this and its apparent relative inferiority as a larvalnutritional substrate (Bridges, 1983; Goldhammer et al., 1990; Coppedge et al.,

BEETLES, FUNGI, AND MITES 89

1995), C. ranaculosus appears to be of less value as a symbiont thanEntomocorticium sp. A. Entomocorticium sp. A, grows more slowly than C.runaculosus, but can grow and provide nutrition for D. frontalis larvae, evenwhen surrounded by 0. minus. Establishing a viable culture of Entomocorticiumsp. A (apparently the most beneficial of the two mycangial fungi) may be a keyto larval D. frontalis success. It is within this complex of competitiveinteractions that the phoretic mites appear to play their most significant role.

Despite their nebulous benefits as symbionts, both 0. minus and C.ranuculosus are maintained within the D. frontalis system. This may belargely due to the role of Tursonemus ips and T. kruntzi as vectors of these twofungi. Tellingly, neither of these mites have ever been found to transportEntomocorticium sp. A. This dichotomy may be due to the different benefitsaccrued by the mite in exchange for vectoring these fungi. Both of these mitescan successfully reproduce, and their offspring thrive (larval survival to firstreproduction approximately equal to 90%), on colonies of 0. minus. Both miteshave positive growth rates when feeding upon new hyphal growth of the 0;minus and C. runuculosus. However, neither of these mites have significantpopulation growth when feeding on the fungus they do not transport,Entomocorticium sp. A. In addition, field observations show that over ten timesthe number of Tursonemus sp. mites are found within patches of 0. minusinfested phloem vs. other areas (Lombardero et al., 2000).

Thus, in this interaction, the mites play the role of facilitators of asymbiotic relationship by virtue of maintaining their own symbioticrelationship. By transporting certain fungi to serve as substrate for their ownreproduction and development, the Tursonemus mites indirectly influence thedynamics of the interactions between their beetle hosts, the fungi they interactwith, and the tree host which contains them all. A similarly complex, thoughperhaps less highly evolved, relationship is found between a less aggressivebeetle and the fungi and mites it carries.

4 3. The small southern pine engraver

Ips uz~Zsus (Eichoff) (Fig. 4) is often considered along with its frequently co-occurring pine engraver species - Ips culligruphus (Germar) and Ips grundicollis(Eichoff). Together, these three bark beetles cause losses of millions of boardfeet of pine timber, although they usually only attack weakened or dying trees(Connor and Wilkins, 1983). Of the three, I. uzlulsus is one of the less aggressiveand does not frequently kill trees (Mason, 1970). In this bark beetle species, themale initiates the attack, creating a nuptial chamber where he is joined by oneto several females. The females create egg galleries and niches within theinner bark, sealing their eggs in place with bits of inner bark formed into plugs

90 K.D. KLEPZIG ET AL.

Figure 4. Smaller southern pine engraver, Ips az~ulsus, adult.

(Gouger et al., 1975; Moser and Roton, 1971). Once the larvae hatch, they feedin short, broad galleries, greatly enlarged at the distal end (similar to thetypes of galleries created by D. frontalis larvae and markedly dissimilar tothose typically created by other Ips species).

As the larvae develop and eventually pupate, growth of a white, heavilysporulating fungus becomes obvious. This fungus [previously identified as aTubercularieh sp. (Yearian, 1966), and an Ambrosiella sp. (Gouger, 1971)] isconsidered to be in the same genus - Entomocorticium - as the D. frontalismycangial fungus (Sullivan, BT, personal communication). The fungal growth isso abundant that newly formed pupae are covered with spores (Gouger, 1971).In addition, newly emergent beetles graze on the fungal growth (Yearian, 1966).

.

Despite the similarities here to the gallery system, behavior and biology ofD. frontalis, no mycangium has been discovered in I. uvulsus (Gouger, 1971; 6

Gouger et al., 1975). Instead, it has been hypothesized that the mutualisticEntomocorticium sp, is transmitted phoretically (by propagules adhering to thebeetle exoskeleton) or via endozoic transfer (passage of propagules through theintestinal tract) (Gouger, 1971). Evidence does at least provide an indicationthat the mouthparts and digestive system are involved in the transmission ofthis fungus, whether or not a specialized structure exists to carry the spores. Ipsavulsus guts contain a mixture of spores, starch, and fine grained tree tissues.Adult males and females both deposit gelatinous feces on the roof of the nuptialchamber. While entering trees, adult males pass frass between their

BEETLES, FUNGI, AND MITES 9 1

Figure 5. lps avulsus phoretically carrying the mite Elattoma bennetti on legs.

mouthparts and front legs, compressing the moist phloem with their mouthsbefore expelling it back into the gallery. While ovipositing, adult females usetheir mouthparts to close the end of each egg niche with a phloem plug(Gouger, 1971).

Regardless of this apparent dissimilarity in the mode of fungal transmission,there are some striking similarities in the manner in which both D. fvontalisand I. avuZsus interact with their fungal (and mite) symbionts. As in the D.frontalis system, 1. avulsus carries a bluestain fungus - Ophiostoma ips(Rumbold) Nannf. - and there are apparently competitive interactions betweenthis fungus and the nutritional mutualist of I. avulsus larvae (Yearian, 1966;Yearian et al., 1972). The interaction here seems to involve interference withlarval mycophagy by the Ophiostoma sp. Wild populations (with their fullmycoflora complement) are significantly more fecund and successful than arefungus free or 0. ips infested populations (Yearian et al., 1972). Much as in the0. minus/D. fiontalis interaction, 0. ips renders pine logs unsuitable as breedingmaterial for I. avulsus (Yearian, 1966). Areas fully colonized by the bluestainfungus become essentially unsuitable for beetle reproduction (although a fewlarvae may feed and survive). The dependence of I. avulsus larvae on theirfungal mutualist is not obligatory, however. It is possible to successfully(although at a much reduced level of success) rear 1. avulsus minus their fungalmutualist. These two beetles are also similar in the manner in which theyinteract with phoretic mites.

92 K.D. KLEPZIG ET AL.

Figure6. Elattoma bennetti. A) Feeding on symbiotic fungus of lps avulsus, and B)physogastr ic female ( lef t ) , ruptured female with newly emerged brood (r ight) .

Ips U~U~SUS is associated with a number of mite species (approximately)equal to that found associated with D. frontalis. Of these species, at least 13are phoretic (Moser and Roton, 1971). One of the more noteworthy andbiologically interesting mites associated with 1. avulsus is Elattoma bennetti

BEETLES, FUNGI, AND MITES 93

(Fig. 5). We have observed this mite feeding within the Entomocorticium sp.lined galleries of I. avtlZsus (Fig. 6a). As the females feed they becomephysogastric (massively swollen) and thus more noticeable within thegalleries (Fig. 6b). The female E. bennetti continue to feed and swell,nourishing developing larval mites within their abdomens. These developingmites mate while still inside the parent female who, after prolonged feedingand swelling, ruptures to give birth to reproductively mature adult mites (Fig.6b). These mites are then ready to be carried phoretically to the next tree (andnext source of Entomocorticium sp.) by emerging I. avulsus. As in the D. frontalissystem, there is a high degree of dependence by a phoretic mite on thesymbiotic fungus of its bark beetle host. The degree to which the mite affectsthe beetle-fungus relationship is unclear, although the possibility certainlyexists for the mite to vector the fungus. At the very least, the life cycles of allthree organisms are tightly interwoven, even interdependent.

4. Discussion

The interactions we have discussed here share several commonalities. Bothinteractions involve three very taxonomically distinct groups in tightly linkedrelationships. Both interactions involve intricate specializations on the partof the symbionts, whether morphological, physiological or behavioral, tomaintain these interactions. Both interactions occur within the context ofecologically and economically important forest pest systems. And bothinteractions require novel research approaches to unravel the complexitieswithin. These relationships may be best understood by considering, in amultidisciplinary fashion, the manner in which symbioses vary with time andresources, and the degree to which other species may affect interactions amongsymbionts. The similarities and differences between, and details of, theseinteractions may have implications to other arthropod-fungus symbioses aswell.

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